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ARTICLE Effect of a prior bout of preconditioning exercise on muscle damage from downhill walking Appl. Physiol. Nutr. Metab. Downloaded from www.nrcresearchpress.com by San Diego (UCSD) on 06/06/15 For personal use only.
Sumiaki Maeo, Yusuke Ochi, Masayoshi Yamamoto, Hiroaki Kanehisa, and Kazunori Nosaka
Abstract: This study investigated whether reduced-duration downhill walking (DW) would confer a protective effect against muscle damage induced by a subsequent bout of longer duration DW performed 1 week or 4 weeks later. Healthy young adults were allocated to a control or one of the preconditioning exercise (PRE-1wk or PRE-4wk) groups (10 men and 4 women per group). PRE-1wk and PRE-4wk groups performed 20-min DW (–28% slope, 5 km/h, 10% body mass added to a backpack) 1 week and 4 weeks before 40-min DW, respectively, and the control group performed 40-min DW only. Maximal voluntary contraction (MVC) knee extension torque, plasma creatine kinase (CK) activity, and muscle soreness (100-mm visual analog scale) were measured before, immediately after, and 24, 48, and 72 h after DW, and the changes in these variables were compared among groups. The control group showed symptoms of muscle damage (e.g., prolonged decrease in MVC: –14% ± 10% at 48 h post-DW) after 40-min DW. Changes in all variables after 40-min DW of PRE-1wk and PRE-4wk groups were 54%–61% smaller (P < 0.05) than the control group, without significant differences between PRE-1wk and PRE-4wk groups for MVC and plasma CK activity. Importantly, changes after the preconditioning exercise (20-min DW) were 67%–69% smaller (P < 0.05) than those after the 40-min DW of the control group. These findings suggest that 20-min DW resulting in minor muscle damage conferred a protective effect against subsequent 40-min DW, and its effect could last for more than 4 weeks. Key words: eccentric exercise, knee extensors, trekking, hiking, maximum strength, creatine kinase activity, muscle soreness, protective effect. Résumé : Cette étude examine la thèse selon laquelle la diminution de la durée d’une marche en descente (« DW ») procure une protection contre les lésions musculaires suscitées par une DW subséquente d’une plus longue durée effectuée 1 semaine ou 4 semaines plus tard. On répartit de jeunes adultes en bonne santé entre un groupe de contrôle et des groupes de préconditionnement par l’exercice suivant : « PRE-1wk » ou « PRE-4wk » (10 hommes et 4 femmes par groupe). Les groupes PRE-1wk et PRE-4wk effectuent 20 min de DW (pente de –28%, 5 km/h, charge de 10% ajoutée au sac a` dos), et ce, 1 semaine et 4 semaines respectivement avant 40 min de DW; le groupe de contrôle effectue seulement 40 min de DW. On évalue le moment de force suscitée par une contraction volontaire maximale des extenseurs du genou (« MVC »), l’activité plasmatique de la créatine kinase (« CK ») et la douleur musculaire (échelle visuelle analogie de 100 mm), et ce, avant, immédiatement après et 24, 48 et 72 h après DW, puis on compare les variations d’un groupe a` l’autre. Le groupe de contrôle présente des symptômes de lésion musculaire (p. ex., diminution prolongée de MVC : –14 ± 10% 48 h post-DW) a` la suite de 40 min de DW. Les modifications de toutes les variables après 40 min de DW dans les groupes PRE-1wk et PRE-4wk sont plus faibles de 54 a` 61% (P < 0,05) comparativement au groupe de contrôle; les différences de MVC et d’activité plasmatique de CK entre les groupes PRE-1wk et PRE-4wk ne sont pas statistiquement significatives. Fait a` noter, les variations a` la suite du préconditionnement par l’exercice (20 min de DW) sont plus faibles de 67 a` 69% (P < 0,05) que dans le groupe de contrôle après 40 min de DW. D’après ces observations, 20 min de DW suscitant des lésions musculaires mineures procurent une protection durant la DW subséquente de 40 min et cette protection pourrait s’étendre sur plus de 4 semaines. [Traduit par la Rédaction] Mots-clés : exercice pliométrique, extenseurs du genou, randonnée d’aventure, randonnée pédestre, force musculaire maximale, activité de la créatine kinase, douleur musculaire, effet de protection.
Introduction Walking in mountain areas such as trekking or hiking is one of the fastest-growing outdoor activities around the world (Heggie and Heggie 2009). It is reported that approximately 10 million people participated in trekking activities in the year 2011 in Japan (Soukaken 2013), and the number of hikers in the United States increased from 25 million to 35 million in the last decade (Statistica
2013). Mountain trekking involves uphill and downhill walking (DW) on uneven and rugged terrain, giving challenges especially for those who are novices or who do it infrequently (Howatson et al. 2011). During DW, knee extensor muscles predominantly perform eccentric contractions, where the force is produced while muscletendon complex is lengthened (Eston et al. 1995). It is well known that eccentric contractions induce muscle damage that is mani-
Received 11 September 2014. Accepted 15 November 2014. S. Maeo. Sports and Life Science, National Institute of Fitness and Sports in Kanoya, 1 Shiromizu, Kanoya, Kagoshima 891-2393, Japan; Japan Society for the Promotion of Science, Kouji, Tokyo 102-0088, Japan; School of Exercise and Health Sciences, Centre for Exercise and Sports Science Research, Edith Cowan University, Joondalup, WA 6027, Australia. Y. Ochi, M. Yamamoto, and H. Kanehisa. Sports and Life Science, National Institute of Fitness and Sports in Kanoya, 1 Shiromizu, Kanoya, Kagoshima 891-2393, Japan. K. Nosaka. School of Exercise and Health Sciences, Centre for Exercise and Sports Science Research, Edith Cowan University, Joondalup, WA 6027, Australia. Corresponding author: Sumiaki Maeo (e-mail: [email protected]). Appl. Physiol. Nutr. Metab. 40: 274–279 (2015) dx.doi.org/10.1139/apnm-2014-0390
Published at www.nrcresearchpress.com/apnm on 19 November 2014.
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festing as reduced muscle function, delayed onset muscle soreness, increased muscular stiffness, and decreased exercise economy, which lasts for several days after exercise, when it is performed for the first time or with a long interval from the previous bout (Byrne et al. 2004). Indeed, previous studies have shown that DW induces muscle damage that lasts for several days (Eston et al. 2000; Ahmadi et al. 2008; Maeo et al. 2015). It has been stated that falling-related accidents and fatalities during mountain trekking are attributable to DW-induced muscle damage in combination with accumulative fatigue from uphill walking (Yamamoto and Yamazaki 2003; Heggie and Heggie 2009). Therefore, it is of importance to develop an intervention that reduces DW-induced muscle damage during mountain trekking. Among many potential interventions to reduce or prevent muscle damage, performing a prior bout of eccentric exercise appears to be most cost-effective and efficient in providing a protective effect against a subsequent bout of potentially damaging eccentric exercise (Howatson and van Someren 2008). It has been shown that repeated bouts of downhill running separated by 2–6 weeks induced little muscle damage after the second bout (Byrnes et al. 1985; Smith et al. 1998, 2007). Also, Eston et al. (1996) reported that 100 maximal isokinetic eccentric contractions of the knee extensors attenuated muscle damage after downhill running performed 2 weeks later. However, it should be noted that the first exercise bout of these studies induced severe muscle damage indicated by prolonged decreases in muscle function and delayed onset muscle soreness. As mentioned, such muscle damage may increase the risk of injury in various physical activities and/or have a negative impact on adherence and compliance with exercises and physical activities (Lastayo et al. 2013). Thus, establishing a strategy to prevent muscle damage in DW without experiencing severe muscle damage is required. Using a single-joint eccentric exercise model such as elbow flexor eccentric exercise, previous studies have shown that an initial bout of low-intensity eccentric exercise provides a protective effect against subsequent bouts of more demanding eccentric exercise performed within several weeks (Chen et al. 2013a, 2013b). For example, it has been reported that low-intensity (10% of maximal voluntary isometric contraction strength) eccentric contractions were effective for substantially attenuating muscle damage induced by subsequent maximal eccentric contractions of the same muscles performed 1–2 weeks later for the elbow flexors (Chen et al. 2012) and knee extensors (Chen et al. 2013b). It was also shown that 2 or 6 maximal eccentric contractions of the elbow flexors conferred a significant protective effect on muscle damage induced by 24 maximal eccentric contractions of the same muscle performed 2 weeks later (Nosaka et al. 2001b). These findings suggest that performing shorter duration DW (smaller number of eccentric contractions) as a preconditioning exercise could attenuate potential muscle damage induced by subsequent longer duration DW (larger number of eccentric contractions); however, no previous studies have investigated this. Also, it is not known how long such protective effect lasts for DW, if preconditioning exercise provides any protective effect. It is important to investigate the duration of the protective effect for DW to provide practical recommendation when preconditioning exercise should be performed. Therefore, the present study investigated whether a prior bout of 20-min DW would confer a protective effect against muscle damage induced by a subsequent bout of 40-min DW performed either 1 week or 4 weeks later. The protocol of DW (gradient: –28%, velocity: 5 km/h, load: 10% of body mass, duration: 40 min) was based on previous studies (Eston et al. 2000; Rowlands et al. 2001; Farr et al. 2002; Ahmadi et al. 2008), and this study chose halfduration (20 min) DW as the preconditioning exercise assuming that the magnitude of muscle damage induced by 20-min DW would be minor. Reducing the exercise duration to a half was thought to be the first step before setting a much shorter duration
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(e.g., 5 min) or modulating other parameters (i.e., gradient, velocity, load). We hypothesized that 20-min DW would induce minor muscle damage, but confer a strong protective effect on muscle damage induced by 40-min DW performed 1 week later. In addition, based on a previous study (Yamamoto 2000) reporting that if 2 bouts of mountain trekking are performed more than 4 weeks apart, both bouts result in medium to severe muscle soreness, we hypothesized that protective effect by the 20-min DW would not last for 4 weeks.
Materials and methods Subjects Healthy young men (n = 30) and women (n = 12) participated in this study. Their mean (±SD) age, height, and body mass were 20.8 ± 1.4 years, 165.2 ± 6.5 cm, and 60.2 ± 6.1 kg, respectively. None of the subjects had been involved in any type of systematic resistance, aerobic, or flexibility training program, and experienced mountain trekking and/or downhill walking in the past 1 year. This study was approved by the ethics committee of the National Institute of Fitness and Sports in Kanoya and was conducted in accordance with the policy statement regarding the use of human subjects by the Declaration of Helsinki. The subjects visited the laboratory, and were fully informed about the purpose, procedures and possible risks involved in the study, and provided a written informed consent. In a familiarization session that was scheduled 3–7 days prior to the experimental session, they performed DW for 30 s in the same setting for the slope, velocity and load as that of the experimental session, and experienced all measurements. Based on the baseline maximal voluntary isometric contraction (MVC) torque of the knee extensors, the subjects were allocated to a control or 1 of the 2 preconditioning (PRE-1wk and PRE-4wk) groups (n = 14 consisting of 10 men and 4 women per group) by matching the average baseline MVC torque among the groups (194.1 ± 23.4 Nm). DW DW was performed on a treadmill (Quasar Med; HP cosmos, Warwickshire, UK) with the gradient of –28%, velocity of 5 km/h, and a load of 10% body mass added to a typical hiking backpack at their preferred stride length and frequency. PRE-1wk and PRE-4wk groups performed 20-min DW with the same setting of the gradient, velocity, and load as that of the 40-min DW 1 week and 4 weeks before 40-min DW, respectively. The control group performed 40-min DW without performing preconditioning exercise (20-min DW). All DW sessions were supervised by one of the authors. Muscle damage markers Indirect markers of muscle damage shown below were measured before, immediately after, and 24, 48, and 72 h after 20-min DW and 40-min DW (Fig. 1). MVC knee extension torque Torque during MVC of the knee extensors of the right leg was measured using a custom-made dynamometer (S-09010C; Takei, Niigata, Japan) in the same manner previously reported (Maeo et al. 2015). Briefly, each subject sat in an adjustable chair with a support for the back while the hip and knee joints were kept at 90° (full extension: 0°). After performing 2–4 submaximal (50%– 80% MVC) contractions, the subjects performed 2 MVCs with a 1-min rest between trials. The subjects were asked to develop torque gradually over 5 s to reach MVC. Additional trials were performed if the difference in the peak torque of the 2 trials was more than 10%. The trial with the highest peak torque was used for further analysis. Plasma creatine kinase (CK) activity Plasma CK activity was measured by a Reflotron analyzer (Reflotron plus system; F. Hoffmann-La Roche, Basel, Switzerland). Published by NRC Research Press
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Fig. 1. Schematic diagram of the experimental design. The measurements were taken before, immediately after, and 24, 48, and 72 h after 20-min (PRE-1wk and PRE-4wk) and 40-min (all groups) downhill walking (DW).
A 30-L whole blood sample was collected with a capillary pipette from a finger prick to a CK test strip (Reflotron CK Test; F. Hoffmann-La Roche). A pilot study showed that the test–retest reliability of the 2 blood samples taken at the same time was high (CV < 1%), thus the measurement was taken only once for each time point for each subject. The normal reference range is 24– 195 IU/L for this method based on the company information. Muscle soreness The magnitude of muscle soreness at the anterior thigh perceived during squat exercise was assessed using a visual analog scale (VAS) consisting of a 100-mm line representing “no pain” at 1 end (0 mm) and “unbearable pain” at the other (100 mm). Based on Krebs et al. (2007), we categorized the severity of muscle soreness as mild (VAS < 30 mm), moderate (30–70 mm), and severe (>70 mm). The subject was instructed to perform a full squat with the feet being shoulder-width apart and the arms being crossed over the chest, and they rated the level of soreness on the scale by a line (Maeo et al. 2015). Statistical analysis Baseline values for all dependent variables before 20-min DW (PRE-1wk and PRE-4wk groups) and 40-min DW (PRE-1wk, PRE4wk, and the control groups) were compared among the groups by 1-way ANOVA. A 2-way repeated measures ANOVA was used to compare the changes in the variables after 20-min DW between PRE-1wk and PRE-4wk groups, between 20-min DW (pooled data of PRE-1wk and PRE-4wk groups) and 40-min DW of the control group, and the changes after 40-min DW among the 3 groups (PRE-1wk, PRE-4wk, control). When the 2-way ANOVA showed a significant interaction effect, Bonferroni post hoc tests were performed for the comparison between time points for each group and between groups for each time point. A significant level was set at P < 0.05. All data were analyzed using IBM SPSS Statistics for Windows (version 20.0; IBM Corp., Armonk, N.Y., USA). The data are presented as means ± SD.
Results Baseline measurements No significant differences were found in any of the baseline dependent variables among the groups before 20-min DW or 40-min DW. Changes in muscle damage markers following 20-min DW No significant differences in the changes in the dependent variable were evident between PRE-1wk and PRE-4wk groups. Thus, the 2-group data were pooled and are shown in Table 1. MVC torque decreased (9.8%, P < 0.05) immediately post-DW, but returned to the baseline by 24 h post-DW. Plasma CK activity and muscle soreness (VAS) significantly increased (peak: 155 IU/L and 23 mm, respectively) at 24–48 h, but returned to the baseline by
48–72 h post-DW. These changes were 67%–69% smaller when compared with those after the 40-min DW of the control group (P < 0.05). Any of these variables for the control group did not return to the baseline by 72 h after 40-min DW, and severe muscle soreness was induced (over 70 mm at 24 and 48 h post-DW). Changes in muscle damage markers following 40-min DW Changes in MVC torque, plasma CK activity, and muscle soreness (VAS) before and after 40-min DW are shown in Fig. 2. MVC torque decreased immediately post-DW for all groups (P < 0.05), but its magnitude was smaller for PRE-1wk and PRE-4wk than the control group at all time points (P < 0.05), without significant difference between PRE-1wk and PRE-4wk groups (Fig. 2a). MVC torque recovered to the baseline by 24 h post-DW for PRE-1wk and PRE-4wk groups, but was still lower than the baseline at 72 h post-DW for the control group. Plasma CK activity increased for all groups (P < 0.05), but its magnitude was smaller for PRE-1wk and PRE-4wk than the control group at 24, 48, and 72 h post-DW (P < 0.05), without significant difference between PRE-1wk and PRE-4wk groups (Fig. 2b). VAS of muscle soreness increased for all groups (P < 0.05), but its magnitude was smaller (P < 0.05) for PRE-1wk and PRE-4wk when compared with the control group at 24, 48, and 72 h post-DW (Fig. 2c). Significant differences were also found between PRE-1wk and PRE-4wk groups at 24 and 48 h post-DW. Muscle soreness disappeared by 72 h for PRE-1wk, but still existed at 72 h post-DW for PRE-4wk and the control groups.
Discussion The results indicated that 20-min DW with lower muscle damage significantly attenuated the magnitude of muscle damage induced by 40-min DW performed 1 week or 4 weeks later. The protective effects were similar between PRE-1wk and PRE-4wk in MVC torque and plasma CK activity. These results supported the hypothesis that 20-min DW would confer a strong protective effect on muscle damage induced by 40-min DW performed 1 week later, but refuted the other hypothesis that the protective effect would not last for 4 weeks. After the 20-min DW, all dependent variables changed significantly, but their magnitudes of changes were small such that MVC torque decreased only at immediately post-DW by 10%, and recovered to the baseline by 24 h post-DW (Table 1). Plasma CK activity did not exceed the normal reference range (24–195 IU/L), and mild muscle soreness lasted only for 48 h post-DW. In contrast, after 40-min DW of the control group, larger changes in the variables were found such that the MVC torque decreased immediately post-DW by 30% and remained lower than the baseline for 72 h post-DW. Plasma CK activity and VAS of muscle soreness showed greater increases than those after 20-min DW, and did not recover at 72 h post-DW. These changes were similar to those observed in Published by NRC Research Press
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Table 1. Changes (mean± SD) in maximal voluntary isometric contraction (MVC) torque of the knee extensors, plasma creatine kinase (CK) activity, and muscle soreness assessed by a 100-mm visual analog scale (VAS) before (Pre), immediately after (0 h), and 24, 48, and 72 h after 20-min downhill walking (pooled data of PRE-1wk and PRE-4wk groups, n = 28) and 40-min downhill walking of the control group (n = 14).
MVC (Nm) 20-min 40-min CK (IU/L) 20-min 40-min VAS (mm) 20-min 40-min
Pre
0h
24 h
48 h
72 h
201.2±21.3 191.0±17.5
181.5±22.4* 134.3±25.5*,†
195.2±19.2 154.5±21.2*,†
197.7±19.1 164.2±20.2*,†
201.9±20.3 173.4±21.5*,†
108.8±62.0 90.5±64.3
111.9±63.3 88.9±65.0
155.1±60.4* 310.9±170.5*,†
140.4±59.3 459.1±195.5*,†
138.1±70.3 471.5±213.5*,†
0.0±0.0 0.0±0.0
1.5±3.7 4.2±8.4
22.8±15.3* 71.2±15.2*,†
19.0±17.0* 73.4±19.8*,†
9.0±14.4 45.9±24.3*,†
*Significant (P < 0.05) difference from the pre-exercise value. †Significant (P < 0.05) difference between groups.
Fig. 2. Changes in maximal voluntary isometric contraction (MVC) torque of the knee extensors (a), plasma creatine kinase (CK) activity (b), and muscle soreness of the anterior thigh assessed by a visual analog scale (VAS; c) before (Pre), immediately after (0), and 24, 48, and 72 h after 40-min downhill walking. Values are means ± SD. *, Significant (P < 0.05) difference from the pre-value (baseline); †, significant (P < 0.05) difference between groups based on a 2-way ANOVA.
the previous studies (Eston et al. 2000; Rowlands et al. 2001; Farr et al. 2002; Ahmadi et al. 2008), in which 40- or 45-min DW was performed without any preconditioning exercise. Thus, the magnitude of muscle damage induced by 40-min DW shown by the control group appeared typical for that without preconditioning exercise. It is important to note that increasing the exercise duration from 20 min to 40 min increased the magnitude of muscle damage more than 2 times. For PRE-1wk and PRE-4wk groups, changes in all dependent variables after 40-min DW were significantly smaller than those for the control group (Fig. 2). This indicates that 20-min DW conferred a protective effect against potential muscle damage induced by 40-min DW. To the best of our knowledge, the present study is the first to show the protective effect conferred by lessdemanding DW on more-demanding DW. It is interesting to note that the magnitudes of the changes in muscle damage markers following 40-min DW for PRE-1wk were similar to those observed in our recent study in which 40-min DW was repeated with a 1-week interval (Maeo et al. 2015). In that study (Maeo et al. 2015),
the first bout of 40-min DW resulted in similar changes in the muscle damage markers as shown by the control group, but the second bout of 40-min DW performed 1 week later resulted in much smaller changes in the markers, which were similar to those observed after 40-min DW in the PRE-1wk group. This suggests that 20-min DW was as effective as 40-min DW to attenuate muscle damage after subsequent 40-min DW performed 1 week later. Contrary to the hypothesis, the present study found that the protective effect conferred by 20-min DW lasted for 4 weeks. In this study, PRE-1wk and PRE-4wk similarly attenuated changes in muscle damage markers induced by 40-min DW, except for muscle soreness that was greater for PRE-4wk than PRE-1wk. From the present study, it is not known how long the protective effect conferred by 20-min DW could last maximally, but considering no differences between PRE-1wk and PRE-4wk groups for the changes in MVC torque and plasma CK activity, it seems likely that the effect could last more than 4 weeks for these variables. A significant difference in muscle soreness between PRE-1wk and PRE-4wk Published by NRC Research Press
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groups indicates that the protective effect of 20-min DW on muscle soreness was attenuated between 1 week and 4 weeks. This may suggest that the protective effect of DW for muscle soreness disappears faster than other muscle damage markers. A previous study (Yamamoto 2000) also showed that if 2 bouts of mountain trekking were performed more than 4 weeks apart, both bouts resulted in medium to severe muscle soreness. In contrast, Chen et al. (2012) reported that the protective effect of low-intensity elbow flexion eccentric exercise remained longer on muscle soreness than other variables. It is uncertain whether this inconsistency was attributed to the difference in the exercise model (i.e., isolated eccentric elbow flexion vs. DW). Further research is needed to clarify this. It should also be noted that the magnitude of muscle damage judged by muscle soreness does not match with that determined by loss of muscle function or increases in plasma CK activity (Newton et al. 2008). Thus, preconditioning exercise effect on muscle soreness should be considered separately from its effect on other aspects of muscle damage (e.g., loss of muscle function). The disparity between muscle soreness and function may have practical implications for athletes when designing a training program since the current result together with the previous finding suggests that muscle soreness may not be a limiting factor in performance. As possible mechanisms underpinning the repeated bout effect or protective effect induced by a single bout of eccentric exercise, McHugh (2003) suggested a combination of neural, mechanical, and cellular adaptations. Neural adaptations include a more homogeneous distribution of the mechanical stress on muscular fibers recruited during exercise, possibly reducing damage of fast-twitch myofibrils that are selectively recruited during eccentric contractions (Warren et al. 2000). Regarding mechanical adaptations, it has been suggested that passive and/or dynamic muscle stiffness increases after the first eccentric bout, which reduces muscle strain in subsequent bouts (McHugh 2003). Penailillo et al. (2014) recently reported that fascicle elongation (strain) during eccentric exercise was 16% less in the second than the first bout. Cellular adaptations include an increase in the number of sarcomeres in series that reduces muscle strain thereby limiting the myofibrillar disruption (Lynn et al. 1998; Butterfield et al. 2005). It is also possible that adaptations in excitation–contraction coupling (e.g., strengthening of sarcoplasmic reticulum) and inflammatory responses (e.g., decreased increases in neutrophils and monocytes) are associated with the repeated bout (McHugh 2003). It is not known how the muscle damage after 40-min DW was attenuated by the prior bout of 20-min DW, thus warranting further studies to investigate the mechanisms. The present study used reduced-duration (20-min) DW as a preconditioning exercise, and its protective effect was found to last for 4 weeks for strength and plasma CK activity, and attenuates between 1 week and 4 weeks for muscle soreness. Chen et al. (2012) reported that a protective effect by low-intensity preconditioning exercise remained for 2 weeks but not 3 weeks. On the other hand, Nosaka et al. (2001a) reported that when the first bout was performed with maximal intensity and high repetition, which induced high degree of muscle damage, protective effects lasted for 6 months. These results indicate that how long the protective effect lasts largely depends on the degree of muscle damage induced by the first session (preconditioning exercise). From the practical perspective, it is reasonable to assume that performing less-demanding DW at least 4 weeks beforehand is a good strategy to minimize muscle damage when planning to go mountain trekking. However, exercise intensity during mountain trekking is changed by several factors (e.g., backpack load, gradient, velocity), and it is not known how much protective effect can be conferred and how long it can last when these variables are modulated in preconditioning intervention. It is important to clarify what should be modulated in preconditioning DW to be most effective. Future research should aim to clarify what factor (e.g., duration,
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load, gradient, or velocity) most influences the muscle damage and/or confers a protective effect on DW to provide more practical recommendations. Also, actual mountain trekking consists of not only downhill but also uphill walking, and usually takes much longer duration ranging from several hours to sometimes more than a day to complete it. Further research is needed to examine these to establish a strategy to attenuate or prevent muscle damage in mountain trekking activities. It should be noted that the present study used young men and women, thus the current results might not be generalized to other populations such as elderly people, who account for large portion of mountain trekkers (Yamamoto and Yamazaki 2003). Also, the participants of the present study had not performed mountain trekking activities for at least 1 year. It is thus assumed that the results would have been somewhat different if experienced or regular mountain trekkers were used in the study. However, a previous study showed that both inexperienced and experienced trekkers similarly perceived muscle soreness after mountain trekking (Yamamoto and Yamazaki 2003), probably because the latter population often takes a more physically challenging and/or longer duration course. Thus, considering that an accident during mountain trekking may directly lead to a serious injury or death in the worst case, the importance of preconditioning exercise should not be underestimated for experienced trekkers as well, since performing preconditioning exercise seems the most effective and efficient strategy to attenuate muscle damage (Howatson and van Someren 2008). In conclusion, this study showed that 20-min DW induced only minor muscle damage, but significantly attenuated muscle damage following 40-min DW performed 1 week or 4 weeks later. The protective effects were similar between PRE-1wk and PRE-4wk in MVC torque and plasma CK activity. These results suggest that preconditioning with reduced-duration DW confers a protective effect on subsequent longer-duration DW, and its effect lasts at least for 4 weeks. Conflict of interest statement The authors declare that there is no conflict of interest and that no companies or manufacturers will benefit from the results of this study.
Acknowledgements This research was supported by a research grant from the Mizuno Foundation for the Promotion of Sports and the Nakatomi Foundation.
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ARTICLE Effect of a prior bout of preconditioning exercise on muscle damage from downhill walking Appl. Physiol. Nutr. Metab. Downloaded from www.nrcresearchpress.com by San Diego (UCSD) on 06/06/15 For personal use only.
Sumiaki Maeo, Yusuke Ochi, Masayoshi Yamamoto, Hiroaki Kanehisa, and Kazunori Nosaka
Abstract: This study investigated whether reduced-duration downhill walking (DW) would confer a protective effect against muscle damage induced by a subsequent bout of longer duration DW performed 1 week or 4 weeks later. Healthy young adults were allocated to a control or one of the preconditioning exercise (PRE-1wk or PRE-4wk) groups (10 men and 4 women per group). PRE-1wk and PRE-4wk groups performed 20-min DW (–28% slope, 5 km/h, 10% body mass added to a backpack) 1 week and 4 weeks before 40-min DW, respectively, and the control group performed 40-min DW only. Maximal voluntary contraction (MVC) knee extension torque, plasma creatine kinase (CK) activity, and muscle soreness (100-mm visual analog scale) were measured before, immediately after, and 24, 48, and 72 h after DW, and the changes in these variables were compared among groups. The control group showed symptoms of muscle damage (e.g., prolonged decrease in MVC: –14% ± 10% at 48 h post-DW) after 40-min DW. Changes in all variables after 40-min DW of PRE-1wk and PRE-4wk groups were 54%–61% smaller (P < 0.05) than the control group, without significant differences between PRE-1wk and PRE-4wk groups for MVC and plasma CK activity. Importantly, changes after the preconditioning exercise (20-min DW) were 67%–69% smaller (P < 0.05) than those after the 40-min DW of the control group. These findings suggest that 20-min DW resulting in minor muscle damage conferred a protective effect against subsequent 40-min DW, and its effect could last for more than 4 weeks. Key words: eccentric exercise, knee extensors, trekking, hiking, maximum strength, creatine kinase activity, muscle soreness, protective effect. Résumé : Cette étude examine la thèse selon laquelle la diminution de la durée d’une marche en descente (« DW ») procure une protection contre les lésions musculaires suscitées par une DW subséquente d’une plus longue durée effectuée 1 semaine ou 4 semaines plus tard. On répartit de jeunes adultes en bonne santé entre un groupe de contrôle et des groupes de préconditionnement par l’exercice suivant : « PRE-1wk » ou « PRE-4wk » (10 hommes et 4 femmes par groupe). Les groupes PRE-1wk et PRE-4wk effectuent 20 min de DW (pente de –28%, 5 km/h, charge de 10% ajoutée au sac a` dos), et ce, 1 semaine et 4 semaines respectivement avant 40 min de DW; le groupe de contrôle effectue seulement 40 min de DW. On évalue le moment de force suscitée par une contraction volontaire maximale des extenseurs du genou (« MVC »), l’activité plasmatique de la créatine kinase (« CK ») et la douleur musculaire (échelle visuelle analogie de 100 mm), et ce, avant, immédiatement après et 24, 48 et 72 h après DW, puis on compare les variations d’un groupe a` l’autre. Le groupe de contrôle présente des symptômes de lésion musculaire (p. ex., diminution prolongée de MVC : –14 ± 10% 48 h post-DW) a` la suite de 40 min de DW. Les modifications de toutes les variables après 40 min de DW dans les groupes PRE-1wk et PRE-4wk sont plus faibles de 54 a` 61% (P < 0,05) comparativement au groupe de contrôle; les différences de MVC et d’activité plasmatique de CK entre les groupes PRE-1wk et PRE-4wk ne sont pas statistiquement significatives. Fait a` noter, les variations a` la suite du préconditionnement par l’exercice (20 min de DW) sont plus faibles de 67 a` 69% (P < 0,05) que dans le groupe de contrôle après 40 min de DW. D’après ces observations, 20 min de DW suscitant des lésions musculaires mineures procurent une protection durant la DW subséquente de 40 min et cette protection pourrait s’étendre sur plus de 4 semaines. [Traduit par la Rédaction] Mots-clés : exercice pliométrique, extenseurs du genou, randonnée d’aventure, randonnée pédestre, force musculaire maximale, activité de la créatine kinase, douleur musculaire, effet de protection.
Introduction Walking in mountain areas such as trekking or hiking is one of the fastest-growing outdoor activities around the world (Heggie and Heggie 2009). It is reported that approximately 10 million people participated in trekking activities in the year 2011 in Japan (Soukaken 2013), and the number of hikers in the United States increased from 25 million to 35 million in the last decade (Statistica
2013). Mountain trekking involves uphill and downhill walking (DW) on uneven and rugged terrain, giving challenges especially for those who are novices or who do it infrequently (Howatson et al. 2011). During DW, knee extensor muscles predominantly perform eccentric contractions, where the force is produced while muscletendon complex is lengthened (Eston et al. 1995). It is well known that eccentric contractions induce muscle damage that is mani-
Received 11 September 2014. Accepted 15 November 2014. S. Maeo. Sports and Life Science, National Institute of Fitness and Sports in Kanoya, 1 Shiromizu, Kanoya, Kagoshima 891-2393, Japan; Japan Society for the Promotion of Science, Kouji, Tokyo 102-0088, Japan; School of Exercise and Health Sciences, Centre for Exercise and Sports Science Research, Edith Cowan University, Joondalup, WA 6027, Australia. Y. Ochi, M. Yamamoto, and H. Kanehisa. Sports and Life Science, National Institute of Fitness and Sports in Kanoya, 1 Shiromizu, Kanoya, Kagoshima 891-2393, Japan. K. Nosaka. School of Exercise and Health Sciences, Centre for Exercise and Sports Science Research, Edith Cowan University, Joondalup, WA 6027, Australia. Corresponding author: Sumiaki Maeo (e-mail: [email protected]). Appl. Physiol. Nutr. Metab. 40: 274–279 (2015) dx.doi.org/10.1139/apnm-2014-0390
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festing as reduced muscle function, delayed onset muscle soreness, increased muscular stiffness, and decreased exercise economy, which lasts for several days after exercise, when it is performed for the first time or with a long interval from the previous bout (Byrne et al. 2004). Indeed, previous studies have shown that DW induces muscle damage that lasts for several days (Eston et al. 2000; Ahmadi et al. 2008; Maeo et al. 2015). It has been stated that falling-related accidents and fatalities during mountain trekking are attributable to DW-induced muscle damage in combination with accumulative fatigue from uphill walking (Yamamoto and Yamazaki 2003; Heggie and Heggie 2009). Therefore, it is of importance to develop an intervention that reduces DW-induced muscle damage during mountain trekking. Among many potential interventions to reduce or prevent muscle damage, performing a prior bout of eccentric exercise appears to be most cost-effective and efficient in providing a protective effect against a subsequent bout of potentially damaging eccentric exercise (Howatson and van Someren 2008). It has been shown that repeated bouts of downhill running separated by 2–6 weeks induced little muscle damage after the second bout (Byrnes et al. 1985; Smith et al. 1998, 2007). Also, Eston et al. (1996) reported that 100 maximal isokinetic eccentric contractions of the knee extensors attenuated muscle damage after downhill running performed 2 weeks later. However, it should be noted that the first exercise bout of these studies induced severe muscle damage indicated by prolonged decreases in muscle function and delayed onset muscle soreness. As mentioned, such muscle damage may increase the risk of injury in various physical activities and/or have a negative impact on adherence and compliance with exercises and physical activities (Lastayo et al. 2013). Thus, establishing a strategy to prevent muscle damage in DW without experiencing severe muscle damage is required. Using a single-joint eccentric exercise model such as elbow flexor eccentric exercise, previous studies have shown that an initial bout of low-intensity eccentric exercise provides a protective effect against subsequent bouts of more demanding eccentric exercise performed within several weeks (Chen et al. 2013a, 2013b). For example, it has been reported that low-intensity (10% of maximal voluntary isometric contraction strength) eccentric contractions were effective for substantially attenuating muscle damage induced by subsequent maximal eccentric contractions of the same muscles performed 1–2 weeks later for the elbow flexors (Chen et al. 2012) and knee extensors (Chen et al. 2013b). It was also shown that 2 or 6 maximal eccentric contractions of the elbow flexors conferred a significant protective effect on muscle damage induced by 24 maximal eccentric contractions of the same muscle performed 2 weeks later (Nosaka et al. 2001b). These findings suggest that performing shorter duration DW (smaller number of eccentric contractions) as a preconditioning exercise could attenuate potential muscle damage induced by subsequent longer duration DW (larger number of eccentric contractions); however, no previous studies have investigated this. Also, it is not known how long such protective effect lasts for DW, if preconditioning exercise provides any protective effect. It is important to investigate the duration of the protective effect for DW to provide practical recommendation when preconditioning exercise should be performed. Therefore, the present study investigated whether a prior bout of 20-min DW would confer a protective effect against muscle damage induced by a subsequent bout of 40-min DW performed either 1 week or 4 weeks later. The protocol of DW (gradient: –28%, velocity: 5 km/h, load: 10% of body mass, duration: 40 min) was based on previous studies (Eston et al. 2000; Rowlands et al. 2001; Farr et al. 2002; Ahmadi et al. 2008), and this study chose halfduration (20 min) DW as the preconditioning exercise assuming that the magnitude of muscle damage induced by 20-min DW would be minor. Reducing the exercise duration to a half was thought to be the first step before setting a much shorter duration
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(e.g., 5 min) or modulating other parameters (i.e., gradient, velocity, load). We hypothesized that 20-min DW would induce minor muscle damage, but confer a strong protective effect on muscle damage induced by 40-min DW performed 1 week later. In addition, based on a previous study (Yamamoto 2000) reporting that if 2 bouts of mountain trekking are performed more than 4 weeks apart, both bouts result in medium to severe muscle soreness, we hypothesized that protective effect by the 20-min DW would not last for 4 weeks.
Materials and methods Subjects Healthy young men (n = 30) and women (n = 12) participated in this study. Their mean (±SD) age, height, and body mass were 20.8 ± 1.4 years, 165.2 ± 6.5 cm, and 60.2 ± 6.1 kg, respectively. None of the subjects had been involved in any type of systematic resistance, aerobic, or flexibility training program, and experienced mountain trekking and/or downhill walking in the past 1 year. This study was approved by the ethics committee of the National Institute of Fitness and Sports in Kanoya and was conducted in accordance with the policy statement regarding the use of human subjects by the Declaration of Helsinki. The subjects visited the laboratory, and were fully informed about the purpose, procedures and possible risks involved in the study, and provided a written informed consent. In a familiarization session that was scheduled 3–7 days prior to the experimental session, they performed DW for 30 s in the same setting for the slope, velocity and load as that of the experimental session, and experienced all measurements. Based on the baseline maximal voluntary isometric contraction (MVC) torque of the knee extensors, the subjects were allocated to a control or 1 of the 2 preconditioning (PRE-1wk and PRE-4wk) groups (n = 14 consisting of 10 men and 4 women per group) by matching the average baseline MVC torque among the groups (194.1 ± 23.4 Nm). DW DW was performed on a treadmill (Quasar Med; HP cosmos, Warwickshire, UK) with the gradient of –28%, velocity of 5 km/h, and a load of 10% body mass added to a typical hiking backpack at their preferred stride length and frequency. PRE-1wk and PRE-4wk groups performed 20-min DW with the same setting of the gradient, velocity, and load as that of the 40-min DW 1 week and 4 weeks before 40-min DW, respectively. The control group performed 40-min DW without performing preconditioning exercise (20-min DW). All DW sessions were supervised by one of the authors. Muscle damage markers Indirect markers of muscle damage shown below were measured before, immediately after, and 24, 48, and 72 h after 20-min DW and 40-min DW (Fig. 1). MVC knee extension torque Torque during MVC of the knee extensors of the right leg was measured using a custom-made dynamometer (S-09010C; Takei, Niigata, Japan) in the same manner previously reported (Maeo et al. 2015). Briefly, each subject sat in an adjustable chair with a support for the back while the hip and knee joints were kept at 90° (full extension: 0°). After performing 2–4 submaximal (50%– 80% MVC) contractions, the subjects performed 2 MVCs with a 1-min rest between trials. The subjects were asked to develop torque gradually over 5 s to reach MVC. Additional trials were performed if the difference in the peak torque of the 2 trials was more than 10%. The trial with the highest peak torque was used for further analysis. Plasma creatine kinase (CK) activity Plasma CK activity was measured by a Reflotron analyzer (Reflotron plus system; F. Hoffmann-La Roche, Basel, Switzerland). Published by NRC Research Press
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Fig. 1. Schematic diagram of the experimental design. The measurements were taken before, immediately after, and 24, 48, and 72 h after 20-min (PRE-1wk and PRE-4wk) and 40-min (all groups) downhill walking (DW).
A 30-L whole blood sample was collected with a capillary pipette from a finger prick to a CK test strip (Reflotron CK Test; F. Hoffmann-La Roche). A pilot study showed that the test–retest reliability of the 2 blood samples taken at the same time was high (CV < 1%), thus the measurement was taken only once for each time point for each subject. The normal reference range is 24– 195 IU/L for this method based on the company information. Muscle soreness The magnitude of muscle soreness at the anterior thigh perceived during squat exercise was assessed using a visual analog scale (VAS) consisting of a 100-mm line representing “no pain” at 1 end (0 mm) and “unbearable pain” at the other (100 mm). Based on Krebs et al. (2007), we categorized the severity of muscle soreness as mild (VAS < 30 mm), moderate (30–70 mm), and severe (>70 mm). The subject was instructed to perform a full squat with the feet being shoulder-width apart and the arms being crossed over the chest, and they rated the level of soreness on the scale by a line (Maeo et al. 2015). Statistical analysis Baseline values for all dependent variables before 20-min DW (PRE-1wk and PRE-4wk groups) and 40-min DW (PRE-1wk, PRE4wk, and the control groups) were compared among the groups by 1-way ANOVA. A 2-way repeated measures ANOVA was used to compare the changes in the variables after 20-min DW between PRE-1wk and PRE-4wk groups, between 20-min DW (pooled data of PRE-1wk and PRE-4wk groups) and 40-min DW of the control group, and the changes after 40-min DW among the 3 groups (PRE-1wk, PRE-4wk, control). When the 2-way ANOVA showed a significant interaction effect, Bonferroni post hoc tests were performed for the comparison between time points for each group and between groups for each time point. A significant level was set at P < 0.05. All data were analyzed using IBM SPSS Statistics for Windows (version 20.0; IBM Corp., Armonk, N.Y., USA). The data are presented as means ± SD.
Results Baseline measurements No significant differences were found in any of the baseline dependent variables among the groups before 20-min DW or 40-min DW. Changes in muscle damage markers following 20-min DW No significant differences in the changes in the dependent variable were evident between PRE-1wk and PRE-4wk groups. Thus, the 2-group data were pooled and are shown in Table 1. MVC torque decreased (9.8%, P < 0.05) immediately post-DW, but returned to the baseline by 24 h post-DW. Plasma CK activity and muscle soreness (VAS) significantly increased (peak: 155 IU/L and 23 mm, respectively) at 24–48 h, but returned to the baseline by
48–72 h post-DW. These changes were 67%–69% smaller when compared with those after the 40-min DW of the control group (P < 0.05). Any of these variables for the control group did not return to the baseline by 72 h after 40-min DW, and severe muscle soreness was induced (over 70 mm at 24 and 48 h post-DW). Changes in muscle damage markers following 40-min DW Changes in MVC torque, plasma CK activity, and muscle soreness (VAS) before and after 40-min DW are shown in Fig. 2. MVC torque decreased immediately post-DW for all groups (P < 0.05), but its magnitude was smaller for PRE-1wk and PRE-4wk than the control group at all time points (P < 0.05), without significant difference between PRE-1wk and PRE-4wk groups (Fig. 2a). MVC torque recovered to the baseline by 24 h post-DW for PRE-1wk and PRE-4wk groups, but was still lower than the baseline at 72 h post-DW for the control group. Plasma CK activity increased for all groups (P < 0.05), but its magnitude was smaller for PRE-1wk and PRE-4wk than the control group at 24, 48, and 72 h post-DW (P < 0.05), without significant difference between PRE-1wk and PRE-4wk groups (Fig. 2b). VAS of muscle soreness increased for all groups (P < 0.05), but its magnitude was smaller (P < 0.05) for PRE-1wk and PRE-4wk when compared with the control group at 24, 48, and 72 h post-DW (Fig. 2c). Significant differences were also found between PRE-1wk and PRE-4wk groups at 24 and 48 h post-DW. Muscle soreness disappeared by 72 h for PRE-1wk, but still existed at 72 h post-DW for PRE-4wk and the control groups.
Discussion The results indicated that 20-min DW with lower muscle damage significantly attenuated the magnitude of muscle damage induced by 40-min DW performed 1 week or 4 weeks later. The protective effects were similar between PRE-1wk and PRE-4wk in MVC torque and plasma CK activity. These results supported the hypothesis that 20-min DW would confer a strong protective effect on muscle damage induced by 40-min DW performed 1 week later, but refuted the other hypothesis that the protective effect would not last for 4 weeks. After the 20-min DW, all dependent variables changed significantly, but their magnitudes of changes were small such that MVC torque decreased only at immediately post-DW by 10%, and recovered to the baseline by 24 h post-DW (Table 1). Plasma CK activity did not exceed the normal reference range (24–195 IU/L), and mild muscle soreness lasted only for 48 h post-DW. In contrast, after 40-min DW of the control group, larger changes in the variables were found such that the MVC torque decreased immediately post-DW by 30% and remained lower than the baseline for 72 h post-DW. Plasma CK activity and VAS of muscle soreness showed greater increases than those after 20-min DW, and did not recover at 72 h post-DW. These changes were similar to those observed in Published by NRC Research Press
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Table 1. Changes (mean± SD) in maximal voluntary isometric contraction (MVC) torque of the knee extensors, plasma creatine kinase (CK) activity, and muscle soreness assessed by a 100-mm visual analog scale (VAS) before (Pre), immediately after (0 h), and 24, 48, and 72 h after 20-min downhill walking (pooled data of PRE-1wk and PRE-4wk groups, n = 28) and 40-min downhill walking of the control group (n = 14).
MVC (Nm) 20-min 40-min CK (IU/L) 20-min 40-min VAS (mm) 20-min 40-min
Pre
0h
24 h
48 h
72 h
201.2±21.3 191.0±17.5
181.5±22.4* 134.3±25.5*,†
195.2±19.2 154.5±21.2*,†
197.7±19.1 164.2±20.2*,†
201.9±20.3 173.4±21.5*,†
108.8±62.0 90.5±64.3
111.9±63.3 88.9±65.0
155.1±60.4* 310.9±170.5*,†
140.4±59.3 459.1±195.5*,†
138.1±70.3 471.5±213.5*,†
0.0±0.0 0.0±0.0
1.5±3.7 4.2±8.4
22.8±15.3* 71.2±15.2*,†
19.0±17.0* 73.4±19.8*,†
9.0±14.4 45.9±24.3*,†
*Significant (P < 0.05) difference from the pre-exercise value. †Significant (P < 0.05) difference between groups.
Fig. 2. Changes in maximal voluntary isometric contraction (MVC) torque of the knee extensors (a), plasma creatine kinase (CK) activity (b), and muscle soreness of the anterior thigh assessed by a visual analog scale (VAS; c) before (Pre), immediately after (0), and 24, 48, and 72 h after 40-min downhill walking. Values are means ± SD. *, Significant (P < 0.05) difference from the pre-value (baseline); †, significant (P < 0.05) difference between groups based on a 2-way ANOVA.
the previous studies (Eston et al. 2000; Rowlands et al. 2001; Farr et al. 2002; Ahmadi et al. 2008), in which 40- or 45-min DW was performed without any preconditioning exercise. Thus, the magnitude of muscle damage induced by 40-min DW shown by the control group appeared typical for that without preconditioning exercise. It is important to note that increasing the exercise duration from 20 min to 40 min increased the magnitude of muscle damage more than 2 times. For PRE-1wk and PRE-4wk groups, changes in all dependent variables after 40-min DW were significantly smaller than those for the control group (Fig. 2). This indicates that 20-min DW conferred a protective effect against potential muscle damage induced by 40-min DW. To the best of our knowledge, the present study is the first to show the protective effect conferred by lessdemanding DW on more-demanding DW. It is interesting to note that the magnitudes of the changes in muscle damage markers following 40-min DW for PRE-1wk were similar to those observed in our recent study in which 40-min DW was repeated with a 1-week interval (Maeo et al. 2015). In that study (Maeo et al. 2015),
the first bout of 40-min DW resulted in similar changes in the muscle damage markers as shown by the control group, but the second bout of 40-min DW performed 1 week later resulted in much smaller changes in the markers, which were similar to those observed after 40-min DW in the PRE-1wk group. This suggests that 20-min DW was as effective as 40-min DW to attenuate muscle damage after subsequent 40-min DW performed 1 week later. Contrary to the hypothesis, the present study found that the protective effect conferred by 20-min DW lasted for 4 weeks. In this study, PRE-1wk and PRE-4wk similarly attenuated changes in muscle damage markers induced by 40-min DW, except for muscle soreness that was greater for PRE-4wk than PRE-1wk. From the present study, it is not known how long the protective effect conferred by 20-min DW could last maximally, but considering no differences between PRE-1wk and PRE-4wk groups for the changes in MVC torque and plasma CK activity, it seems likely that the effect could last more than 4 weeks for these variables. A significant difference in muscle soreness between PRE-1wk and PRE-4wk Published by NRC Research Press
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groups indicates that the protective effect of 20-min DW on muscle soreness was attenuated between 1 week and 4 weeks. This may suggest that the protective effect of DW for muscle soreness disappears faster than other muscle damage markers. A previous study (Yamamoto 2000) also showed that if 2 bouts of mountain trekking were performed more than 4 weeks apart, both bouts resulted in medium to severe muscle soreness. In contrast, Chen et al. (2012) reported that the protective effect of low-intensity elbow flexion eccentric exercise remained longer on muscle soreness than other variables. It is uncertain whether this inconsistency was attributed to the difference in the exercise model (i.e., isolated eccentric elbow flexion vs. DW). Further research is needed to clarify this. It should also be noted that the magnitude of muscle damage judged by muscle soreness does not match with that determined by loss of muscle function or increases in plasma CK activity (Newton et al. 2008). Thus, preconditioning exercise effect on muscle soreness should be considered separately from its effect on other aspects of muscle damage (e.g., loss of muscle function). The disparity between muscle soreness and function may have practical implications for athletes when designing a training program since the current result together with the previous finding suggests that muscle soreness may not be a limiting factor in performance. As possible mechanisms underpinning the repeated bout effect or protective effect induced by a single bout of eccentric exercise, McHugh (2003) suggested a combination of neural, mechanical, and cellular adaptations. Neural adaptations include a more homogeneous distribution of the mechanical stress on muscular fibers recruited during exercise, possibly reducing damage of fast-twitch myofibrils that are selectively recruited during eccentric contractions (Warren et al. 2000). Regarding mechanical adaptations, it has been suggested that passive and/or dynamic muscle stiffness increases after the first eccentric bout, which reduces muscle strain in subsequent bouts (McHugh 2003). Penailillo et al. (2014) recently reported that fascicle elongation (strain) during eccentric exercise was 16% less in the second than the first bout. Cellular adaptations include an increase in the number of sarcomeres in series that reduces muscle strain thereby limiting the myofibrillar disruption (Lynn et al. 1998; Butterfield et al. 2005). It is also possible that adaptations in excitation–contraction coupling (e.g., strengthening of sarcoplasmic reticulum) and inflammatory responses (e.g., decreased increases in neutrophils and monocytes) are associated with the repeated bout (McHugh 2003). It is not known how the muscle damage after 40-min DW was attenuated by the prior bout of 20-min DW, thus warranting further studies to investigate the mechanisms. The present study used reduced-duration (20-min) DW as a preconditioning exercise, and its protective effect was found to last for 4 weeks for strength and plasma CK activity, and attenuates between 1 week and 4 weeks for muscle soreness. Chen et al. (2012) reported that a protective effect by low-intensity preconditioning exercise remained for 2 weeks but not 3 weeks. On the other hand, Nosaka et al. (2001a) reported that when the first bout was performed with maximal intensity and high repetition, which induced high degree of muscle damage, protective effects lasted for 6 months. These results indicate that how long the protective effect lasts largely depends on the degree of muscle damage induced by the first session (preconditioning exercise). From the practical perspective, it is reasonable to assume that performing less-demanding DW at least 4 weeks beforehand is a good strategy to minimize muscle damage when planning to go mountain trekking. However, exercise intensity during mountain trekking is changed by several factors (e.g., backpack load, gradient, velocity), and it is not known how much protective effect can be conferred and how long it can last when these variables are modulated in preconditioning intervention. It is important to clarify what should be modulated in preconditioning DW to be most effective. Future research should aim to clarify what factor (e.g., duration,
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load, gradient, or velocity) most influences the muscle damage and/or confers a protective effect on DW to provide more practical recommendations. Also, actual mountain trekking consists of not only downhill but also uphill walking, and usually takes much longer duration ranging from several hours to sometimes more than a day to complete it. Further research is needed to examine these to establish a strategy to attenuate or prevent muscle damage in mountain trekking activities. It should be noted that the present study used young men and women, thus the current results might not be generalized to other populations such as elderly people, who account for large portion of mountain trekkers (Yamamoto and Yamazaki 2003). Also, the participants of the present study had not performed mountain trekking activities for at least 1 year. It is thus assumed that the results would have been somewhat different if experienced or regular mountain trekkers were used in the study. However, a previous study showed that both inexperienced and experienced trekkers similarly perceived muscle soreness after mountain trekking (Yamamoto and Yamazaki 2003), probably because the latter population often takes a more physically challenging and/or longer duration course. Thus, considering that an accident during mountain trekking may directly lead to a serious injury or death in the worst case, the importance of preconditioning exercise should not be underestimated for experienced trekkers as well, since performing preconditioning exercise seems the most effective and efficient strategy to attenuate muscle damage (Howatson and van Someren 2008). In conclusion, this study showed that 20-min DW induced only minor muscle damage, but significantly attenuated muscle damage following 40-min DW performed 1 week or 4 weeks later. The protective effects were similar between PRE-1wk and PRE-4wk in MVC torque and plasma CK activity. These results suggest that preconditioning with reduced-duration DW confers a protective effect on subsequent longer-duration DW, and its effect lasts at least for 4 weeks. Conflict of interest statement The authors declare that there is no conflict of interest and that no companies or manufacturers will benefit from the results of this study.
Acknowledgements This research was supported by a research grant from the Mizuno Foundation for the Promotion of Sports and the Nakatomi Foundation.
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